The neuronal serum- and glucocorticoid-regulated kinase 1.1 reduces neuronal excitability and protects against seizures through upregulation of the M-current

Journal of Neuroscience

Volumn 33, Issue 6, 2013, Pages 2684-2696

  Miranda, Pablo ^a,b   Cadaveira Mosquera, Alba ^c   González Montelongo, Rafaela ^a,b   Villarroe, Alvaro ^d   González Hernández, Tomás ^b   Lamas, J Antonio ^c   de la Rosa, Diego Alvarez ^b   Giraldez, Teresa ^a  

^a HOSPITAL UNIVERSITARIO NUESTRA SEÑORA DE CANDELARIA   (Spain)

^b UNIVERSIDAD DE LA LAGUNA   (Spain)

^c UNIVERSITY OF VIGO   (Spain)

^d CSIC UPV Unidad de Biofisica UBF   (Spain)

Author keywords

[No Author keywords available]

Indexed keywords

MUSCARINIC RECEPTOR; PHOSPHATIDYLINOSITOL 4, 5 BISPHOSPHATE PHOSPHODIESTERASE; POTASSIUM CHANNEL KV7.2; POTASSIUM CHANNEL KV7.3; SERUM AND GLUCOCORTICOID REGULATED KINASE 1; UNCLASSIFIED DRUG; VOLTAGE GATED POTASSIUM CHANNEL;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; ELECTROPHYSIOLOGY; FLOW CYTOMETRY; GENE EXPRESSION; HUMAN; HUMAN CELL; MOUSE; NERVE CELL EXCITABILITY; NERVE CELL MEMBRANE STEADY POTENTIAL; NEUROPROTECTION; NONHUMAN; NUCLEOTIDE SEQUENCE; POTASSIUM CURRENT; PRIORITY JOURNAL; PROTEIN INTERACTION; PROTEIN LOCALIZATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEIZURE; SPIKE WAVE; SUPERIOR CERVICAL GANGLION; XENOPUS;

ANIMALS; CELLS, CULTURED; FEMALE; HEK293 CELLS; HUMANS; IMMEDIATE-EARLY PROTEINS; KCNQ2 POTASSIUM CHANNEL; KCNQ3 POTASSIUM CHANNEL; MEMBRANE POTENTIALS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURONS; PROTEIN-SERINE-THREONINE KINASES; SEIZURES; UP-REGULATION; XENOPUS LAEVIS;

EID: 84873295534     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.3442-12.2013     Document Type: Article

References (74)

1. Alvarez de la Rosa D, Zhang P, Náray-Fejes-Tóóth A, Fejes-Tóth G, Canessa CM (1999) The serum and glucocorticoid kinase sgk increases the abundance of epithelial sodium channels in the plasma membrane of Xenopus oocytes. J Biol Chem 274:37834-37839. CrossRef Medline
2. Arteaga MF, Alvarez de la Rosa D, Alvarez JA, Canessa CM (2007) Multiple translational isoforms give functional specificity to serum- and glucocorticoid-induced kinase 1. Mol Biol Cell 18:2072-2080. CrossRef Medline
3. Arteaga MF, Coric T, Straub C, Canessa CM (2008) A brain-specific SGK1 splice isoform regulates expression of ASIC1 in neurons. Proc Natl Acad Sci U S A 105:4459-4464. CrossRef Medline
4. + channel gating by activation of a G protein-coupled receptor and protein kinase C. J Physiol 511:333-346. CrossRef Medline
5. Barroso-González J, El Jaber-Vazdekis N, García-Expósito L, Machado JD, Zárate R, Ravelo AG, Estévez-Braun A, Valenzuela-Fernández A (2009) The lupane-type triterpene 30-oxo-calenduladiol is a CCR5 antagonist with anti-HIV-1 and anti-chemotactic activities. J Biol Chem 284:16609-16620. CrossRef Medline
6. Biervert C, Schroeder BC, Kubisch C, Berkovic SF, Propping P, Jentsch TJ, Steinlein OK (1998) A potassium channel mutation in neonatal human epilepsy. Science 279:403-406. CrossRef Medline
7. Brown DA, Adams PR (1980) Muscarinic suppression of a novel voltagesensitive K+ current in a vertebrate neurone. Nature 283:673-676. CrossRef Medline
8. Brunet A, Park J, Tran H, Hu LS, Hemmings BA, Greenberg ME (2001) Protein kinase SGK mediates survival signals by phosphorylating the forkhead transcription factor FKHRL1 (FOXO3a). Mol Cell Biol 21:952-965. CrossRef Medline
9. Buckmaster PS (2004) Laboratory animal models of temporal lobe epilepsy. Comp Med 54:473-485. Medline
10. Cadaveira-Mosquera A, Ribeiro SJ, Reboreda A, Pérez M, Lamas JA (2011) Activation of TREK currents by the neuroprotective agent riluzole in mouse sympathetic neurons. J Neurosci 31:1375-1385. CrossRef Medline
11. Charlier C, Singh NA, Ryan SG, Lewis TB, Reus BE, Leach RJ, Leppert M (1998) A pore mutation in a novel KQT-like potassium channel gene in an idiopathic epilepsy family. Nat Genet 18:53-55. CrossRef Medline
12. Chen X, Zhang X, Jia C, Xu J, Gao H, Zhang G, Du X, Zhang H (2011) Membrane depolarization increases membrane PtdIns(4,5)P2 levels through mechanisms involving PKC βII and PI4 kinase. J Biol Chem 286:39760-39767. CrossRef Medline
13. Debonneville C, Flores SY, Kamynina E, Plant PJ, Tauxe C, Thomas MA, Münster C, Chraïbi A, Pratt JH, Horisberger JD, Pearce D, Loffing J, Staub O (2001) Phosphorylation of Nedd4-2 by Sgk1 regulates epithelial Na(+) channel cell surface expression. EMBO J 20:7052-7059. CrossRef Medline
14. Delmas P, Brown DA (2005) Pathways modulating neural KCNQ/M (Kv7) potassium channels. Nat Rev Neurosci 6:850-862. CrossRef Medline
15. Ekberg J, Schuetz F, Boase NA, Conroy SJ, Manning J, Kumar S, Poronnik P, Adams DJ (2007) Regulation of the voltage-gated K(+) channels KCNQ2/3 and KCNQ3/5 by ubiquitination. Novel role for Nedd4-2. J Biol Chem 282:12135-12142. CrossRef Medline
16. Etxeberria A, Santana-Castro I, Regalado MP, Aivar P, Villarroel A (2004) Three mechanisms underlie KCNQ2/3 heteromeric potassium M-channel potentiation. J Neurosci 24:9146-9152. CrossRef Medline
17. Falkenburger BH, Jensen JB, Hille B (2010a) Kinetics of PIP2 metabolism and KCNQ2/3 channel regulation studied with a voltage-sensitive phosphatase in living cells. J Gen Physiol 135:99-114. CrossRef Medline
18. Falkenburger BH, Jensen JB, Dickson EJ, Suh BC, Hille B (2010b) Phosphoinositides: lipid regulators of membrane proteins. J Physiol 588: 3179-3185. CrossRef Medline
19. Gamper N, Stockand JD, Shapiro MS (2003) Subunit-specific modulation of KCNQ potassium channels by Src tyrosine kinase. J Neurosci 23:84-95. Medline
20. 2+/calmodulin. Mol Biol Cell 16:3538-3551. CrossRef Medline
21. Gehrmann T, Heilmeyer LM Jr (1998) Phosphatidylinositol 4-kinases. Eur J Biochem 253:357-370. CrossRef Medline
22. 2+ oscillations in GH3 rat anterior pituitary cells. Cell Calcium 31:65-78. CrossRef Medline
23. Gómez-Posada JC, Etxeberría A, Roura-Ferrer M, Areso P, Masin M, Murrell-Lagnado RD, Villarroel A (2010) A pore residue of the KCNQ3 potassium M-channel subunit controls surface expression. J Neurosci 30:9316-9323. CrossRef Medline
24. Gómez-Posada JC, Aivar P, Alberdi A, Alaimo A, Etxeberría A, Fernández-Orth J, Zamalloa T, Roura-Ferrer M, Villace P, Areso P, Casis O, Villarroel A (2011) Kv7 channels can function without constitutive calmodulin tethering. PLoS One 6:e25508. CrossRef Medline
25. Gutman GA, Chandy KG, Adelman JP, Aiyar J, Bayliss DA, Clapham DE, Covarriubias M, Desir GV, Furuichi K, Ganetzky B, Garcia ML, Grissmer S, Jan LY, Karschin A, Kim D, Kuperschmidt S, Kurachi Y, Lazdunski M, Lesage F, Lester HA, et al. (2003) International Union of Pharmacology. XLI. Compendium of voltage-gated ion channels: potassium channels. Pharmacol Rev 55:583-586. CrossRef Medline
26. Hadley JK, Passmore GM, Tatulian L, Al-Qatari M, Ye F, Wickenden AD, Brown DA (2003) Stoichiometry of expressed KCNQ2/KCNQ3 potassium channels and subunit composition of native ganglionicMchannels deduced from block by tetraethylammonium. J Neurosci 23:5012-5019. Medline
27. + channel Kv1.3 by the ubiquitin ligase Nedd4-2 and the serum and glucocorticoid inducible kinase SGK1. J Cell Physiol 199:194-199. CrossRef Medline
28. Hernandez CC, Zaika O, Tolstykh GP, Shapiro MS (2008) Regulation of neural KCNQ channels: signalling pathways, structural motifs and functional implications. J Physiol 586:1811-1821. CrossRef Medline
29. Jentsch TJ (2000) Neuronal KCNQ potassium channels: physiology and role in disease. Nat Rev Neurosci 1:21-30. CrossRef Medline
30. Kamynina E, Debonneville C, Bens M, Vandewalle A, Staub O (2001) A novel mouse Nedd4 protein suppresses the activity of the epithelial Na+ channel. FASEB J 15:204-214. CrossRef Medline
31. Kobayashi T, Cohen P (1999) Activation of serum- and glucocorticoid regulated protein kinase by agonists that activate phosphatidylinositide 3-kinase is mediated by 3-phosphoinositide-dependent protein kinase-1 (PDK1) and PDK2. Biochem J 339:319-328. Medline
32. Kosenko A, Kang S, Smith IM, Greene DL, Langeberg LK, Scott JD, Hoshi N (2012) Coordinated signal integration at the M-type potassium channel upon muscarinic stimulation. EMBO J 31:3147-3156. CrossRef Medline
33. Lalioti M, Heath J (2001) A new method for generating point mutations in bacterial artificial chromosomes by homologous recombination in Escherichia coli. Nucleic Acids Res 29:E14. CrossRef Medline
34. Lamas JA (1998) A hyperpolarization-activated cation current (Ih) contributes to resting membrane potential in rat superior cervical sympathetic neurones. Pflugers Arch 436:429-435. CrossRef Medline
35. Lamas JA, Reboreda A, Codesido V (2002) Ionic basis of the resting membrane potential in cultured rat sympathetic neurons. Neuroreport 13: 585-591. CrossRef Medline
36. Lamas JA, Romero M, Reboreda A, Sánchez E, Ribeiro SJ (2009) A riluzoleand valproate-sensitive persistent sodium current contributes to the resting membrane potential and increases the excitability of sympathetic neurones. Pflugers Arch 458:589-599. CrossRef Medline
37. Li Y, Langlais P, Gamper N, Liu F, Shapiro MS (2004) Dual phosphorylations underlie modulation of unitary KCNQ K(+) channels by Src tyrosine kinase. J Biol Chem 279:45399-45407. CrossRef Medline
38. Li Y, Gamper N, Hilgemann DW, Shapiro MS (2005) Regulation of Kv7 (KCNQ) K+ channel open probability by phosphatidylinositol 4,5-bisphosphate. J Neurosci 25:9825-9835. CrossRef Medline
39. Loew LM (2007) Where does all the PIP2 come from? J Physiol 582:945-951. CrossRef Medline
40. Lothman EW, Collins RC (1981) Kainic acid induced limbic seizures: metabolic, behavioral, electroencephalographic and neuropathological correlates. Brain Res 218:299-318. CrossRef Medline
41. Magistretti J, Mantegazza M, de Curtis M, Wanke E (1998) Modalities of distortion of physiological voltage signals by patch-clamp amplifiers: a modeling study. Biophys J 74:831-842. CrossRef Medline
42. Marrion NV (1997) Control of M-current. Annu Rev Physiol 59:483-504. CrossRef Medline
43. Marrion NV, Smart TG, Marsh SJ, Brown DA (1989) Muscarinic suppression of the M-current in the rat sympathetic ganglion is mediated by receptors of the M1-subtype. Br J Pharmacol 98:557-573. CrossRef Medline
44. McCord MC, Lorenzana A, Bloom CS, Chancer ZO, Schauwecker PE (2008) Effect of age on kainate-induced seizure severity and cell death. Neuroscience 154:1143-1153. CrossRef Medline
45. Nakajo K, Kubo Y (2005) Protein kinase C shifts the voltage dependence of KCNQ/M channels expressed in Xenopus oocytes. J Physiol 569:59-74. CrossRef Medline
46. Neher E (1992) Correction for liquid junction potentials in patch clamp experiments. Methods Enzymol 207:123-131. CrossRef Medline
47. Palmada M, Dieter M, Boehmer C, Waldegger S, Lang F (2004) Serum and glucocorticoid inducible kinases functionally regulate ClC-2 channels. Biochem Biophys Res Commun 321:1001-1006. CrossRef Medline
48. Poët M, Kornak U, Schweizer M, Zdebik AA, Scheel O, Hoelter S, Wurst W, Schmitt A, Fuhrmann JC, Planells-Cases R, Mole SE, Hübner CA, Jentsch TJ (2006) Lysosomal storage disease upon disruption of the neuronal chloride transport protein ClC-6. Proc Natl Acad Sci U S A 103:13854-13859. CrossRef Medline
49. Racine RJ (1972) Modification of seizure activity by electrical stimulation. II. Motor seizure. Electroencephalogr Clin Neurophysiol 32:281-294. CrossRef Medline
50. Rae J, Cooper K, Gates P, Watsky M (1991) Low access resistance perforated patch recordings using amphotericin B. J Neurosci Methods 37:15-26. CrossRef Medline
51. Raikwar NS, Snyder PM, Thomas CP (2008) An evolutionarily conserved N-terminal Sgk1 variant with enhanced stability and improved function. Am J Physiol Renal Physiol 295:F1440-F1448. CrossRef Medline
52. Romero M, Reboreda A, Sánchez E, Lamas JA (2004) Newly developed blockers of the M-current do not reduce spike frequency adaptation in cultured mouse sympathetic neurons. Eur J Neurosci 19:2693-2702. CrossRef Medline
53. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3:1101-1108. CrossRef Medline
54. Schroeder BC, Kubisch C, Stein V, Jentsch TJ (1998) Moderate loss of function of cyclic-AMP-modulated KCNQ2/KCNQ3 K+ channels causes epilepsy. Nature 396:687-690. CrossRef Medline
55. Schuetz F, Kumar S, Poronnik P, Adams DJ (2008) Regulation of the voltage-gated K(+) channels KCNQ2/3 and KCNQ3/5 by serum- and glucocorticoid-regulated kinase-1. Am J Physiol Cell Physiol 295:C73-C80. CrossRef Medline
56. Schwake M, Pusch M, Kharkovets T, Jentsch TJ (2000) Surface expression and single channel properties of KCNQ2/KCNQ3, M-type K+ channels involved in epilepsy. J Biol Chem 275:13343-13348. CrossRef Medline
57. Schwake M, Jentsch TJ, Friedrich T (2003) A carboxy-terminal domain determines the subunit specificity of KCNQ K+ channel assembly. EMBO Rep 4:76-81. CrossRef Medline
58. Schwake M, Athanasiadu D, Beimgraben C, Blanz J, Beck C, Jentsch TJ, Saftig P, Friedrich T (2006) Structural determinants of M-type KCNQ (Kv7) K+ channel assembly. J Neurosci 26:3757-3766. CrossRef Medline
59. Schwarz JR, Glassmeier G, Cooper EC, Kao TC, Nodera H, Tabuena D, Kaji R, Bostock H (2006) KCNQ channels mediate IKs, a slow K+ current regulating excitability in the rat node of Ranvier. J Physiol 573:17-34. CrossRef Medline
60. Shapiro MS, Roche JP, Kaftan EJ, Cruzblanca H, Mackie K, Hille B (2000) Reconstitution of muscarinic modulation of the KCNQ2/KCNQ3 K+ channels that underlie the neuronalMcurrent. J Neurosci 20:1710-1721. Medline
61. Singh NA, Charlier C, Stauffer D, DuPont BR, Leach RJ, Melis R, Ronen GM, Bjerre I, Quattlebaum T, Murphy JV, McHarg ML, Gagnon D, Rosales TO, Peiffer A, Anderson VE, Leppert M (1998) A novel potassium channel gene, KCNQ2, is mutated in an inherited epilepsy of newborns. Nat Genet 18:25-29. CrossRef Medline
62. Snyder PM, Olson DR, Thomas BC (2002) Serum and glucocorticoidregulated kinase modulates Nedd4-2-mediated inhibition of the epithelial Na+ channel. J Biol Chem 277:5-8. CrossRef Medline
63. Staub O, Dho S, Henry P, Correa J, Ishikawa T, McGlade J, Rotin D (1996) WWdomains of Nedd4 bind to the proline-rich PY motifs in the epithe-lial Na+ channel deleted in Liddle's syndrome. EMBO J 15:2371-2380. Medline
64. Suh BC, Hille B (2002) Recovery from muscarinic modulation of Mcurrent channels requires phosphatidylinositol 4,5-bisphosphate synthesis. Neuron 35:507-520. CrossRef Medline
65. Tinel N, Diochot S, Lauritzen I, Barhanin J, Lazdunski M, Borsotto M (2000) M-type KCNQ2-KCNQ3 potassium channels are modulated by the KCNE2 subunit. FEBS Lett 480:137-141. CrossRef Medline
66. Tzingounis AV, Nicoll RA (2008) Contribution of KCNQ2 and KCNQ3 to the medium and slow afterhyperpolarization currents. Proc Natl Acad Sci U S A 105:19974-19979. CrossRef Medline
67. Wang HS, Pan Z, Shi W, Brown BS, Wymore RS, Cohen IS, Dixon JE, McKinnon D (1998) KCNQ2 and KCNQ3 potassium channel subunits: molecular correlates of the M-channel. Science 282:1890-1893. CrossRef Medline
68. Wesch D, Miranda P, Afonso-Oramas D, Althaus M, Castro-Hernández J, Dominguez J, Morty RE, Clauss W, González-Hernández T, Alvarez de la Rosa D, Giraldez T (2010) The neuronal-specific SGK1.1 kinase regulates {delta}-epithelial Na+ channel independently of PY motifs and couples it to phospholipase C signaling. Am J Physiol Cell Physiol 299:C779-C790. CrossRef Medline
69. Wesch D, Althaus M, Miranda P, Cruz-Muros I, Fronius M, González-Hernández T, Clauss WG, Alvarez de la Rosa D, Giraldez T (2012) Differential N termini in epithelial Na+ channel δ-subunit isoforms modulate channel trafficking to the membrane. Am J Physiol Cell Physiol 302:C868-C879. CrossRef Medline
70. Winks JS, Hughes S, Filippov AK, Tatulian L, Abogadie FC, Brown DA, Marsh SJ (2005) Relationship between membrane phosphatidylinositol-4,5-bisphosphate and receptor-mediated inhibition of native neuronal M channels. J Neurosci 25:3400-3413. CrossRef Medline
71. Zaika O, Lara LS, Gamper N, Hilgemann DW, Jaffe DB, Shapiro MS (2006) Angiotensin II regulates neuronal excitability via phosphatidylinositol 4,5-bisphosphate-dependent modulation of Kv7 (M-type) K+ channels. J Physiol 575:49-67. CrossRef Medline
72. Zaika O, Hernandez CC, Bal M, Tolstykh GP, Shapiro MS (2008) Determinants within the turret and pore-loop domains of KCNQ3 K+ channels governing functional activity. Biophys J 95:5121-5137. CrossRef Medline
73. Zhang H, Craciun LC, Mirshahi T, Rohács T, Lopes CM, Jin T, Logothetis DE (2003) PIP(2) activates KCNQ channels, and its hydrolysis underlies receptor-mediated inhibition of M currents. Neuron 37:963-975. CrossRef Medline
74. Zhang X, Chen X, Jia C, Geng X, Du X, Zhang H (2010) Depolarization increases phosphatidylinositol (PI) 4,5-bisphosphate level and KCNQ currents through PI 4-kinase mechanisms. J Biol Chem 285:9402-9409. CrossRef Medline